Innervation of monkey extraocular muscles: Localization of sensory and motor neurons by retrograde transport of horseradish peroxidase

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Abstract
Neurons that provide sensory and motor innervation of extraocular muscles in the monkey have been identified and localized by retrograde transport of horseradish peroxidase (HRP). Injections of HRP into individual extraocular muscles of rhesus or pig‐tail monkeys labeled pseudounipolar neurons that were localized within the ipsilateral semilunar ganglion. The distribution of labeled neurons within the ganglion was consistent with its somatotopic organization as the majority were found within the ophthalmic subdivision. Absence of labeled neurons within either the trigeminal mesencephalic or spinal nucleus was in agreement with previous findings in the cat (Porter and Spencer, '82). Intracranial transection of the ophthalmic nerve prior to muscle injection eliminated all labeling within the ganglion. These data indicate that the extraocular muscles can be selectively deafferented in order to examine the potential role(s) of proprioception in the neural control of eye movements.Injections of HRP into the extraocular muscles also resulted in the la beling of individual motoneuron populations. Each extraocular muscle was found to receive solely unilateral innervation, with contralateral representation of only the superior rectus and superior oblique. Within the oculomotor nucleus there was a moderate topographic segregation of individual motoneuron populations. Primate medial rectus and inferior rectus representations, while at variance with the classical descriptions (Warwick, '53), were consistent with those obtained in contemporary tracer studies (Büttner Ennever and Akert, '81; Spencer and Porter, '81). Superior rectus motoneurons were distributed along the medial aspect of the contralateral nucleus, with the predominant representation at caudal to midnuclear levels. Inferior oblique motoneurons filled the gap lateral to those of the superior rectus and ventral to medial rectus (dorsal subgroup) and inferior rectus representations at their respective levels. Following injections of the lateral rectus and superior oblique labeled motoneurons were found within the ipsilateral abducens nucleus and contralateral trochlear nucleus, respectively. Superior oblique motoneurons were strictly confined to the well‐defined neuronal borders of the trochlear nucleus. Those innervating the lateral rectus, in addition to lying within the abducens proper, extended ventrolaterally from the nucleus to form a discrete ventral abducens nucleus. Our data provide a complete description of the innervation pattern of primate extraocular muscles which is based upon contemporary tracer techniques. These findings include the first demonstration of the localization of monkey first‐order afferent neurons which subserve extraocular muscle proprioception.

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